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In this study, we report the coding-complete genome sequence of Grapevine leafroll-associated virus 13 (GLRaV-13), isolate CA8881, detected in Vitis vinifera in California, USA. The genome sequence exhibited over 95% nucleotide identity with previously reported GLRaV-13 isolates and contributed to better understanding of the genetic diversity of ampeloviruses infecting grapevine.
Ampelographic collections play an important role in the conservation of grapevine genetic resources and therefore require continuous phytosanitary monitoring. In this study, the virome of grapevines from the Magarach ampelographic collection in Russia was analyzed using total RNA high-throughput sequencing. A total of twenty-seven grapevine viruses and four viroids were identified. Two viruses were characterized as putative novel species: (+) ssRNA grapevine umbra-like virus 5 (GULV-5) and the bipartite (+) ssRNA grapevine Magarach secovirus (GMSV), which, together with related viruses, may represent a novel genus within the family Secoviridae. Among the economically important viruses, the most prevalent were grapevine fanleaf virus (76%), grapevine leafroll-associated virus 1 (39%), and grapevine virus A (33%). Mixed infections involving two or three of these viruses were detected in 50% of the analyzed grapevines. Grapevine virus D was detected in Russia for the first time. Phylogenetic analysis of 222 assembled virus and viroid genome sequences revealed high genetic diversity. The obtained results were summarized and compared with previous virome studies conducted on four Russian ampelographic collections.
Viticulture became central to most Mediterranean civilizations a few millennia after the grapevine (Vitis vinifera L.) was domesticated in the South Caucasus/Near East. To elucidate the origins of the grapevines that enabled this westward spread over the past 3,000 years, we analyzed 28 grapevine seeds from seven archaeological sites in the Iberian Peninsula and Sardinia. Ancient DNA recovered from the oldest seeds with domesticated-like morphology (from ∼1,000 BCE), found in southwestern Spain, revealed nuclear and chloroplast genome signatures of Eastern Mediterranean cultivars. Seeds from the same and later Iron Age Iberian sites, however, showed genomic signatures suggesting hybridization between local wild grapevines and eastern-origin cultivars. The genetic makeup of Sardinian and northeastern Spanish seeds supports that local diversification giving rise to the Central European and Iberian wine genetic lineages had already occurred in the early Iron Age. In Iberia, Roman-period seeds were first-degree related to both the earliest eastern-introduced domesticates and a Medieval seed whose genetic makeup matches the extant Iberian variety "Pasa Valenciana." Another Medieval seed was inferred as an offspring of the extant "Heben," indicating that this major founder of Iberian germplasm has been continuously propagated for over 1,100 years. Our results confirm previous evolutionary models indicating that Western Mediterranean viticulture began with introductions of eastern domesticated grapevines, followed by early hybridization with local Iberian wild grapevines that may have facilitated viticulture adaptation to the new environment. The aDNA unveils that these introductions gave rise to extant cultivars through only a few sexual generations and long-term reliance on clonal propagation.
Climate change is broadly expected to increase the range of many plant diseases, yet the current status of local thermal adaptation in many pathogens is poorly understood. Xylella fastidiosa (Xf) is a global bacterial plant pathogen that causes Pierce's disease (PD) of grapevines and infects over 700 other host plant species, impacting both agricultural and natural ecosystems. In a common garden experiment with 477 vines in the field, we compared PD outcomes from a local (colder climate in CA) vs non-local (warmer climate in CA) bacterial strain in 13 Mediterranean grapevine varieties over 3 years. Relative to the local strain, there was 77% lower overwinter survival in the non-local strain from a warmer climate, strongly indicating local adaptation in these CA Xf populations. Host genotype also had a significant effect on pathogen winter survival, and grapevine varieties differed in PD susceptibility. Additionally, we assessed in planta evolution of the two pathogen strains over 3 years by whole-genome sequencing 58 field-derived isolates. There were convergent loss-of-function mutations in genes encoding minor Type IV pilin (T4P) proteins, which control twitching motility and other virulence phenotypes, suggesting rapid adaptive evolution. Our results suggest local adaptation to cold temperatures in a bacterial plant pathogen and a possible role for minor Type IV pilins in thermal adaptation. These findings demonstrate the urgent need to incorporate X. fastidiosa evolution and local thermal adaptation into global models of PD spread. Differentiating pathotypes with distinct thermal adaptations will improve disease forecasting and inform quarantine decisions.IMPORTANCEForecasting the movement of plant pathogens is a critical issue under global warming to effectively manage future plant disease outbreaks. Yet, current plant pathogen local thermal adaptation is often unaccounted for, especially in bacterial pathogens. Our study examines local adaptation to temperature in a bacterial plant pathogen, Xylella fastidiosa, that causes disease in grapevines in addition to infecting 700 other plant species. In a large-scale field experiment across 13 grapevine varieties, we demonstrate local adaptation in pathogen winter survival in distinct Xylella fastidiosa strains. Additionally, we found evidence of adaptive evolution in just 3 years, as we observed convergent mutations after resequencing strains that evolved in the field. Our results suggest that X. fastidiosa populations-even within a small geographic area-have distinct adaptations to winter temperatures and may exhibit differential responses to warming winters.
Hormone signaling and MADS-box genes regulate grapevine tendril and inflorescence growth divergence, offering molecular insights for managing tendril growth. Grapevine (Vitis vinifera L.) tendrils and inflorescences are homologous organs; however, their divergent development has important agronomic consequences because excessive tendril growth increases vineyard management costs. To explore the regulatory mechanisms, we compared the inflorescence-prone cultivar 'Einset Seedless' (ENT) with the tendril-prone cultivar 'Pinot Noir' (PN) using anatomical observation, transcriptome analysis of specific tendril nodes, and functional characterization of MADS-box genes. ENT exhibited a higher flowering rate at tendril nodes 1-4 than PN. Transcriptome profiling of specific tendril nodes uncovered 549 differentially expressed genes (DEGs) through an intersection/exclusion strategy, with Kyoto Encyclopedia of Genes and Genomes (KEGG) enrichment indicating that hormone and mitogen-activated protein kinase (MAPK) signaling were the primary candidates driving the divergence. To assess the spatiotemporal dynamics of these DEGs, we performed Mfuzz clustering, which revealed that multiple expression trajectories were highly consistent with the flowering gradient across different ENT and PN nodes. Plant hormone signal transduction was the predominantly enriched pathway across all dynamic clusters, highlighting the centrality of phytohormones in this process. Guided by this transcriptional evidence, we measured endogenous zeatin and gibberellin (GA₃) contents in the nodal tissues. Remarkably, the zeatin-to-GA₃ ratio not only paralleled the flowering gradient but also correlated with the cluster expression trajectories, providing physiological evidence for a cytokinin-gibberellin interaction model governing organ divergence. Additionally, we analyzed the differentially expressed transcription factors among the DEGs and identified a MADS-box gene, FRUITFULL-LIKE (VvFUL-L), which was markedly upregulated in PN tendrils. Heterologous overexpression of VvFUL-L in arabidopsis promoted early flowering and reduced inflorescence branching, suggesting its potential role in regulating lateral meristem development and affecting tendril formation. Collectively, these findings establish that Hormone Signaling, particularly cytokinin-GA crosstalk, and MADS-box regulators, such as VvFUL-L, are key regulators of inflorescence versus tendril growth in grapevines, providing a basis for future molecular and breeding studies.
Pangenomes have now been developed for several horticultural crops, yet the extent to which genome diversity in sequence and organization contribute to plant adaptation and major agronomic traits remains poorly understood. Here, we assembled the genomes of 9 cultivated grapevine varieties and compared the genomes of 15 cultivated grapevine varieties for variation in gene and TE content. We found that genomic collinearity is highly conserved among varieties. We still observed substantial variation across genomes. Notably, we identified across varieties 55,662 orthologous genes, of which 55.3% appears to be dispensable. Dispensable genes are enriched for functions related to adaptation to biotic and abiotic constraints, suggesting that they may play a role in adaptation. Comparing our results with a recently published study, we found substantial differences with ∼12.6% of the genes we classified as core genes being classified as dispensable genes in this other study. We then constructed a pangenome graph and used it to performed genome-wide association studies for 3 important traits in grapevine production, which allowed us to include large structural variants as markers in the analyses. We identified 32 loci that we did not detect when we used the PN40024 genome as a reference, 20 of which are newly reported associations. Overall, our results indicates that despite recent advances in characterizing plant pangenomes, current gene classification into core and dispensable gene categories should be taken with caution. They also highlight the value of incorporating structural variants into GWAS, to better characterize the genetic architecture of agronomic traits.
The implementation of genome editing strategies in grapevine is the easiest way to improve sustainability and resilience while preserving the original genotype. Among others, the Mildew Locus-O (MLO) genes have already been reported as good candidates to develop powdery mildew-immune plants. A never-explored grapevine target is NPR3, a negative regulator of the systemic acquired resistance. We report the exploitation of a cisgenic approach with the Cre-lox recombinase technology to generate grapevine-edited plants with the potential to be transgene-free while preserving their original genetic background. The characterization of three edited lines for each target demonstrated immunity development against Erysiphe necator in MLO6-7-edited plants. Concomitantly, a significant improvement of resilience, associated with increased leaf thickness and specific biochemical responses, was observed in defective NPR3 lines against E. necator and Plasmopara viticola. Transcriptomic analysis revealed that both MLO6-7 and NPR3 defective lines modulated their gene expression profiles, pointing to distinct though partially overlapping responses. Furthermore, targeted metabolite analysis highlighted an overaccumulation of stilbenes coupled with an improved oxidative scavenging potential in both editing targets, likely protecting the MLO6-7 mutants from detrimental pleiotropic effects. Finally, the Cre-loxP approach allowed the recovery of one MLO6-7 edited plant with the complete removal of transgene. Taken together, our achievements provide a comprehensive understanding of the molecular and biochemical adjustments occurring in double MLO-defective grape plants. In parallel, the potential of NPR3 mutants for multiple purposes has been demonstrated, raising new questions on its wide role in orchestrating biotic stress responses.
Grapevine cultivars vary widely in monoterpenoid content, yet the genetic and regulatory mechanisms underlying this variation remain poorly characterized beyond highly aromatic Muscat types. We profiled free volatiles and monoterpenoid glycosides in a Riesling × Cabernet Sauvignon F1 mapping population, revealing extensive variation and transgressive segregation consistent with multigenic control. QTL mapping identified 70 significant loci associated with 48 volatile compounds and monoterpene glycosides, including two major QTLs explaining 33.6% and 33.4% of phenotypic variance in (3S)-linalool accumulation. Integration of haplotype-resolved transcriptomics with metabolite data, enabled by a chromosome-scale diploid Riesling genome assembly, resolved a (3S)-linalool/nerolidol synthase cluster on chromosome 10 and identified VviTPS54 as the strongest candidate underlying linalool variation. VviTPS54 exhibited haplotype-specific expression strongly correlated with (3S)-linalool accumulation across genotypes, while no QTL was detected at the 1-deoxy-D-xylulose-5-phosphate synthase 1 (VviDXS1) locus previously identified in Muscat cultivars. In addition, VviDXS1 expression was not correlated with terpene levels, indicating that regulatory variation within terpene synthase clusters, rather than methylerythritol phosphate (MEP) pathway flux, drives monoterpenoid composition in this population. These results establish regulatory variation of terpene synthases as a key mechanism underlying monoterpenoid diversity in grapevine and demonstrate that resolving such variation requires haplotype-phased genome assemblies coupled with haplotype-resolved transcriptomics to detect allele-specific expression differences at complex, heterozygous loci.
Haplotype-resolved genome assemblies were produced for Chasselas and Ugni Blanc, two heterozygous Vitis vinifera cultivars by combining high-fidelity long-read sequencing and high-throughput chromosome conformation capture (Hi-C). The telomere-to-telomere full coverage of the chromosomes allowed us to assemble separately the two haplo-genomes of both cultivars and revealed structural variations between the two haplotypes of a given cultivar. The deletions/insertions, inversions, translocations, and duplications provide insight into the evolutionary history and parental relationship among grape varieties. Integration of de novo single long-read sequencing of full-length transcript isoforms (Iso-Seq) yielded a highly improved genome annotation. Given its higher contiguity, and the robustness of the IsoSeq-based annotation, the Chasselas assembly meets the standard to become the annotated reference genome for V. vinifera. Building on these resources, we developed VitExpress, an open interactive transcriptomic platform, that provides a genome browser and integrated web tools for expression profiling, and a set of statistical tools (StatTools) for the identification of highly correlated genes. Implementation of the correlation finder tool for MybA1, a major regulator of the anthocyanin pathway, identified candidate genes associated with anthocyanin metabolism, whose expression patterns were experimentally validated as discriminating between black and white grapes. These resources and innovative tools for mining genome-related data are anticipated to foster advances in several areas of grapevine research.
Mediterranean regions are among the most important areas for global grape production, characterized by dry climates and frequent challenges associated with soil salinity. In these environments, chloride toxicity is a major factor limiting vine growth and fruit quality. Despite the critical role of chloride exclusion in salinity tolerance, the genetic mechanisms underlying this trait remain poorly understood. In this study, we analyzed natural variation in chloride exclusion using a diverse panel of 335 accessions representing 18 wild and cultivated Vitis species. This panel, comprising accessions from the southwestern United States and Mexico, captures a broad range of evolutionary adaptations to abiotic stress and provides a valuable genetic resource for breeding efforts aimed at introducing novel traits. Using genome-wide association and quantitative trait loci (QTL) mapping, we identified a major QTL on chromosome 8, now designated qClEx8.1, containing candidate genes encoding cation/H⁺ exchangers (CHXs), which are involved in ion transport and homeostasis. To validate these findings, we analyzed a mapping population derived from Vitis acerifolia longii 9018 and the commercial rootstock GRN3, confirming the chromosome 8 locus as a major determinant of chloride exclusion. Structural variant analysis revealed nonsynonymous substitutions within CHX genes that may influence protein function and salinity tolerance. Additionally, we discovered a novel QTL on chromosome 19 enriched with G-type lectin S-receptor-like serine/threonine-protein kinases, known regulators of stress signaling. By integrating phenotypic and genomic data across a diverse Vitis collection, this study advances our understanding of the genetic architecture underlying chloride exclusion and highlights candidate genes for breeding salt-tolerant rootstocks.
Xylella fastidiosa is a plant-pathogenic bacterium that causes severe diseases in economically important crops, such as citrus and grapevine, thereby posing a significant threat to global agriculture. Although X. fastidiosa has not yet been reported in Korea, the increase in international trade and its presence in neighboring countries highlight the necessity of continued surveillance. The objective of this study was to verify the absence of X. fastidiosa in Korea and to establish a reliable diagnostic framework through a nationwide survey conducted in 2024 and 2025. The sampling design was generated using the RiBESS+ statistical model to ensure the reliability of the survey results. Host plants, including grapevines (Vitis vinifera), mandarin oranges (Citrus unshiu), and cherry blossoms (Prunus yedoensis), were selected and sampled from urban and agricultural areas throughout the country for a nationwide survey. Genomic DNA was extracted from plant petioles and analyzed using real-time PCR with an optimized primer set (XF16S-F/R). Over a period of two years, a total of 2,314 samples were collected, exceeding the required sample size of 843 per year. X. fastidiosa was not detected in any of the collected and tested samples. These results confirm the absence of X. fastidiosa in Korea throughout the study period with high statistical confidence. This study provides evidence confirming the absence of X. fastidiosa in Korea and proposes a standardized methodology for future surveillance and early detection of other invasive prohibited quarantine pests.
The host range of Agrobacterium tumefaciens 1D1109, known to induce crown gall only on grapevine (Vitis spp.), was extended to include many plant species by transferring a tumor-inducing plasmid (pTi) from strain 1D1, a broad-host-range pathogen. The pTi plasmid was mobilized by the conjugative plasmid pRK2, which was inserted into 1D1 by mating with Escherichia coli J53(pRK2). The resulting transconjugants were screened for their ability to induce crown gall tumors on hosts other than grapevine by inoculation into sunflower. Transconjugants that were virulent on sunflower were then tested on 36 different host plants and compared with host-limited strain 1D1109 and the donor strain. Two transconjugants induced tumors on the same 28 plant species as those of the original plasmid donor 1D1(pRK2) (pTi). These results show that pRK2 promoted transfer of the pTi plasmid and suggest that the pTi plasmid rather than the A. tumefaciens chromosome determined the host range of the pathogen. Insertion of pRK2 alone did not extend the host range of strain 1D1109. Insertion of pS-a into A. tumefaciens 1D1 by mating with E. coli J53-1 (pS-a) resulted in the concomitant loss of pTi and virulence. There appears to be incompatibility between pTi and pS-a.
Pedunculate oak (Quercus robur L.) is a foundation tree species in European forests and reforestation programs, but nursery propagated seedlings can harbor cryptic trunk diseases pathogens. Cadophora luteo-olivacea, known from grapevine trunk diseases, has been detected in oak nurseries, yet its pathogenicity on oak and interactions with antagonistic fungi remain unclear. We fulfilled Koch's postulates for C. luteo-olivacea isolate CZ_395 on Q. robur seedlings under experimental inoculation conditions and quantified growth reduction of C. luteo-olivacea by Trichoderma atroviride isolate CZ_180 in dual culture. Proteomic and metabolomic profiling of the contact zone was performed at two post contact sampling points, 4 and 8 dpi, to identify candidate molecular signatures associated with the interaction. Inoculated seedlings developed extensive stem lesions (mean 11.9 cm), whereas controls showed minimal wound response (mean 0.9 cm; p < 0.001). In dual culture, T. atroviride reduced the visible colony development and radial growth of C. luteo-olivacea under the tested in vitro conditions. Contact zone proteomics revealed 257 differentially abundant proteins at 8 days, including cell wall targeting hydrolases, secreted proteases, oxidoreductases (44 upregulated), and transporters. Metabolomics detected contact specific changes in amino acids, central carbon intermediates, and lipid-associated features, including reduced ergosterol. This study demonstrates that C. luteo-olivacea can induce necrotic lesions in Q. robur under experimental inoculation conditions and identifies proteomic and metabolomic signatures associated with the interaction between T. atroviride and C. luteo-olivacea, providing a basis for nursery risk assessment and future evaluation of biocontrol potential.
MOTIVATION: Structural variations (SVs), including inversions, translocations (TRAs), duplications, and large insertions or deletions, are key drivers of genome evolution and phenotypic diversity. With the increasing number of high-quality, chromosome-scale genome assemblies, the ability to detect and interpret SVs has become a crucial aspect of modern genomics. While SV detection has advanced, most visualization methods produce static plots that fall short when researchers, particularly in comparative genomics, need to interactively explore large datasets, zoom into specific genomic regions, or dynamically filter structural events in real time. RESULTS: To address this gap, we introduce SynFlow, a lightweight, web-based interactive application specifically designed for exploring and visualizing SVs identified by SyRI. We demonstrate that SynFlow can reproduce complex static synteny plots published in literature, but transforms them into dynamic, shareable visualizations that support real-time filtering, reordering, and deep exploration of specific SVs, including TRAs. SynFlow is available as a web server and offers multiple entry points: browsing precomputed datasets (e.g. banana and grapevine genomes), uploading user-provided SyRI outputs, or running an integrated workflow to produce and visualize SVs on the fly. AVAILABILITY AND IMPLEMENTATION: https://synflow.southgreen.fr; source code https://github.com/SouthGreenPlatform/synflow; preprocessing Snakemake workflow https://gitlab.cirad.fr/agap/cluster/snakemake/synflow.
CRISPR ribonucleoprotein (RNP)-mediated genome editing offers a transgene-free platform for precise genetic modification in diverse herbaceous and tree species, including rice, wheat, apple, poplar, oil palm, rubber tree and grapevine. However, its application in woody plants faces distinct challenges, notably inefficient delivery and regeneration difficulties, particularly in species such as bamboo. While some of these issues also occur in herbaceous plants, they are often significantly more complex in woody species due to factors such as intricate cell wall architecture, widespread recalcitrant genotypes and inherent limitations of current delivery platforms. This review presents the first in-depth, critical re-evaluation of recent advancements in RNP-mediated editing in woody plants, highlighting these obstacles that warrant focused attention. Unlike plasmid-based CRISPR systems, RNP editing utilises Cas9/Cas12a protein-guide RNA complexes without integrating foreign DNA. This enables a DNA-free editing strategy that simplifies regulatory approval and minimises off-target effects due to the transient presence and rapid degradation of RNPs within plant cells. While PEG-mediated protoplast transfection and particle bombardment remain the primary reported methods for RNP delivery in trees, we evaluate promising alternative strategies such as lipofection, electroporation, cell-penetrating peptides and nanoparticle-based systems for targeted RNP delivery. Despite their promise, these advanced methods remain largely untested in woody species. Finally, we outline future research directions, including the development of tree-specific RNP delivery systems and regeneration protocols to enhance efficiency and minimise cytotoxicity. These innovations are essential for unlocking the full potential of RNP-mediated genome editing in long-lived tree species. This review provides a focused and timely roadmap for expanding the application of RNP technology across diverse woody plants.